Background Among women infected with the human immunodeficiencyvirus (HIV), there is a high prevalence of human papillomavirus(HPV) infections. However, little is known about the naturalhistory of HPV infections in HIV-seropositive women, and persistentHPV infections may explain the increased risk of cervical squamousintraepithelial lesions and invasive cervical cancer in HIV-seropositivewomen.
Methods A total of 220 HIV-seropositive and 231 HIV-seronegativewomen in the New York City area were evaluated at two or moresemiannual gynecologic examinations that included a Pap test,a test for HPV DNA, and colposcopy.
Results HPV DNA was detected at the initial examination in 56percent of the HIV-seropositive and 31 percent of the HIV-seronegativewomen. After four examinations, the cumulative prevalence ofHPV infection was 83 percent in the seropositive women and 62percent in the seronegative women (P<0.001). Persistent HPVinfections were found in 24 percent of the seropositive womenbut in only 4 percent of the seronegative women (P<0.001).Twenty percent of the seropositive women and 3 percent of theseronegative women had persistent infections with HPV-16associatedviral types (16, 31, 33, 35, or 58) or HPV-18associatedtypes (18 or 45) (P<0.001), which are most strongly associatedwith cervical cancer. The detection of HPV DNA in women withpreviously negative tests was not associated with sexual activityduring the interval since the preceding examination.
Conclusions HIV-seropositive women have a high rate of persistentHPV infections with the types of HPV that are strongly associatedwith the development of high-grade squamous intraepitheliallesions and invasive cervical cancer. These persistent infectionsmay explain the increased incidence of squamous intraepitheliallesions in HIV-seropositive women.
Source Information
From the Department of Pathology, College of Physicians and Surgeons (X.-W.S., T.C.W.), and the Gertrude H. Sergievsky Center and Division of Epidemiology (L.K.), Columbia University, New York; the Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta (T.V.E., T.J.B.); and the Bureau of Disease Intervention Research, New York City Department of Health, New York (M.A.C.).
Address reprint requests to Dr. Wright at the Department of Pathology, Room 16-402, College of Physicians and Surgeons, Columbia University, 630 W. 168th St., New York, NY 10032.
Chaturvedi, A. K., Madeleine, M. M., Biggar, R. J., Engels, E. A.
(2009). Risk of Human Papillomavirus-Associated Cancers Among Persons With AIDS. JNCI J Natl Cancer Inst
101: 1120-1130
[Abstract][Full Text]
Whitaker, J. M., Palefsky, J. M., Da Costa, M., King, C. M., Johnston, J. S., Barbosa, P.
(2009). Human Papilloma Virus Type 69 Identified in a Clinically Aggressive Plantar Verruca from an HIV-positive Patient. J. Am. Podiatr. Med. Assoc.
99: 8-12
[Abstract][Full Text]
Tornesello, M. L., Duraturo, M. L., Giorgi-Rossi, P., Sansone, M., Piccoli, R., Buonaguro, L., Buonaguro, F. M.
(2008). Human papillomavirus (HPV) genotypes and HPV16 variants in human immunodeficiency virus-positive Italian women. J. Gen. Virol.
89: 1380-1389
[Abstract][Full Text]
Safaeian, M., Kiddugavu, M., Gravitt, P. E., Gange, S. J., Ssekasanvu, J., Murokora, D., Sklar, M., Serwadda, D., Wawer, M. J., Shah, K. V., Gray, R.
(2008). Determinants of Incidence and Clearance of High-Risk Human Papillomavirus Infections in Rural Rakai, Uganda. Cancer Epidemiol. Biomarkers Prev.
17: 1300-1307
[Abstract][Full Text]
Vaccarella, S., Herrero, R., Snijders, P. J F, Dai, M., Thomas, J. O, Hieu, N. T., Ferreccio, C., Matos, E., Posso, H., de Sanjose, S., Shin, H. R., Sukvirach, S., Lazcano-Ponce, E., Munoz, N., Meijer, C. J L M, Franceschi, S., the IARC HPV Prevalence Surveys (IHPS) Study Group,
(2008). Smoking and human papillomavirus infection: pooled analysis of the International Agency for Research on Cancer HPV Prevalence Surveys. Int J Epidemiol
37: 536-546
[Abstract][Full Text]
Echchannaoui, H., Bianchi, M., Baud, D., Bobst, M., Stehle, J.-C., Nardelli-Haefliger, D.
(2008). Intravaginal Immunization of Mice with Recombinant Salmonella enterica Serovar Typhimurium Expressing Human Papillomavirus Type 16 Antigens as a Potential Route of Vaccination against Cervical Cancer. Infect. Immun.
76: 1940-1951
[Abstract][Full Text]
Sirera, G., Videla, S., Lopez-Blazquez, R., Llatjos, M., Tarrats, A., Castella, E., Grane, N., Tural, C., Rey-Joly, C., Clotet, B.
(2008). Highly active antiretroviral therapy and incidence of cervical squamous intraepithelial lesions among HIV-infected women with normal cytology and CD4 counts above 350 cells/mm3. J Antimicrob Chemother
61: 191-194
[Abstract][Full Text]
Burns, J., Shaknovich, R., Lau, J., Haramati, L. B.
(2007). Oncogenic Viruses in AIDS: Mechanisms of Disease and Intrathoracic Manifestations. Am. J. Roentgenol.
189: 1082-1087
[Abstract][Full Text]
Kim, J. J., Kuntz, K. M., Stout, N. K., Mahmud, S., Villa, L. L., Franco, E. L., Goldie, S. J.
(2007). Multiparameter Calibration of a Natural History Model of Cervical Cancer. Am J Epidemiol
166: 137-150
[Abstract][Full Text]
Tohill, B. C, Heilig, C. M, Klein, R. S, Rompalo, A., Cu-Uvin, S., Piwoz, E. G, Jamieson, D. J, Duerr, A.
(2007). Nutritional biomarkers associated with gynecological conditions among US women with or at risk of HIV infection. Am. J. Clin. Nutr.
85: 1327-1334
[Abstract][Full Text]
Gunnell, A. S., Tran, T. N., Torrang, A., Dickman, P. W., Sparen, P., Palmgren, J., Ylitalo, N.
(2006). Synergy between Cigarette Smoking and Human Papillomavirus Type 16 in Cervical Cancer In situ Development. Cancer Epidemiol. Biomarkers Prev.
15: 2141-2147
[Abstract][Full Text]
Koshiol, J., Schroeder, J., Jamieson, D. J., Marshall, S. W., Duerr, A., Heilig, C. M., Shah, K. V., Klein, R. S., Cu-Uvin, S., Schuman, P., Celentano, D., Smith, J. S.
(2006). Smoking and Time to Clearance of Human Papillomavirus Infection in HIV-Seropositive and HIV-Seronegative Women. Am J Epidemiol
164: 176-183
[Abstract][Full Text]
Silverberg, M. J., Schneider, M. F., Silver, B., Anastos, K. M., Burk, R. D., Minkoff, H., Palefsky, J., Levine, A. M., Viscidi, R. P.
(2006). Serological Detection of Human Papillomavirus Type 16 Infection in Human Immunodeficiency Virus (HIV)-Positive and High-Risk HIV-Negative Women. CVI
13: 511-519
[Abstract][Full Text]
Smits, P. H. M., Bakker, R., Jong, E., Mulder, J. W., Meenhorst, P. L., Kleter, B., van Doorn, L.-J., Quint, W. G. V.
(2005). High Prevalence of Human Papillomavirus Infections in Urine Samples from Human Immunodeficiency Virus-Infected Men. J. Clin. Microbiol.
43: 5936-5939
[Abstract][Full Text]
Bodaghi, S., Wood, L. V., Roby, G., Ryder, C., Steinberg, S. M., Zheng, Z.-M.
(2005). Could Human Papillomaviruses Be Spread through Blood?. J. Clin. Microbiol.
43: 5428-5434
[Abstract][Full Text]
Kim, J. J., Wright, T. C., Goldie, S. J.
(2005). Cost-effectiveness of Human Papillomavirus DNA Testing in the United Kingdom, The Netherlands, France, and Italy. JNCI J Natl Cancer Inst
97: 888-895
[Abstract][Full Text]
Strickler, H. D., Burk, R. D., Fazzari, M., Anastos, K., Minkoff, H., Massad, L. S., Hall, C., Bacon, M., Levine, A. M., Watts, D. H., Silverberg, M. J., Xue, X., Schlecht, N. F., Melnick, S., Palefsky, J. M.
(2005). Natural History and Possible Reactivation of Human Papillomavirus in Human Immunodeficiency Virus-Positive Women. JNCI J Natl Cancer Inst
97: 577-586
[Abstract][Full Text]
Walker, F., Adle-Biassette, H., Madelenat, P., Henin, D., Lehy, T.
(2005). Increased Apoptosis in Cervical Intraepithelial Neoplasia Associated with HIV Infection: Implication of Oncogenic Human Papillomavirus, Caspases, and Langerhans Cells. Clin. Cancer Res.
11: 2451-2458
[Abstract][Full Text]
Villada, I. B., Barracco, M. M., Ziol, M., Chaboissier, A., Barget, N., Berville, S., Paniel, B., Jullian, E., Clerici, T., Maillere, B., Guillet, J. G.
(2004). Spontaneous Regression of Grade 3 Vulvar Intraepithelial Neoplasia Associated with Human Papillomavirus-16-Specific CD4+ and CD8+ T-Cell Responses. Cancer Res.
64: 8761-8766
[Abstract][Full Text]
Xi, L. F., Kiviat, N. B.
(2004). Cervical Neoplasia and Highly Active Antiretroviral Therapy. JNCI J Natl Cancer Inst
96: 1051-1053
[Full Text]
Ahdieh-Grant, L., Li, R., Levine, A. M., Massad, L. S., Strickler, H. D., Minkoff, H., Moxley, M., Palefsky, J., Sacks, H., Burk, R. D., Gange, S. J.
(2004). Highly Active Antiretroviral Therapy and Cervical Squamous Intraepithelial Lesions in Human Immunodeficiency Virus-Positive Women. JNCI J Natl Cancer Inst
96: 1070-1076
[Abstract][Full Text]
Chaturvedi, A. K., Brinkman, J. A., Gaffga, A. M., Dumestre, J., Clark, R. A., Braly, P. S., Dunlap, K., Kissinger, P. J., Hagensee, M. E.
(2004). Distribution of human papillomavirus type 16 variants in human immunodeficiency virus type 1-positive and -negative women. J. Gen. Virol.
85: 1237-1241
[Abstract][Full Text]
Goldie, S. J., Kohli, M., Grima, D., Weinstein, M. C., Wright, T. C., Bosch, F. X., Franco, E.
(2004). Projected Clinical Benefits and Cost-effectiveness of a Human Papillomavirus 16/18 Vaccine. JNCI J Natl Cancer Inst
96: 604-615
[Abstract][Full Text]
Taylor, G., Wolff, T., Khanna, N., Furth, P., Langenberg, P.
(2004). Genital Dysplasia in Women Infected with Human Immunodeficiency Virus. J Am Board Fam Med
17: 108-113
[Abstract][Full Text]
Ferenczy, A., Coutlee, F., Franco, E., Hankins, C.
(2003). Human papillomavirus and HIV coinfection and the risk of neoplasias of the lower genital tract: a review of recent developments. CMAJ
169: 431-434
[Abstract][Full Text]
Palefsky, J. M., Holly, E. A.
(2003). Chapter 6: Immunosuppression and Co-infection with HIV. J Natl Cancer Inst Monogr
2003: 41-46
[Abstract][Full Text]
Cameron, J. E., Snowhite, I. V., Chaturvedi, A. K., Hagensee, M. E.
(2003). Human Papillomavirus-Specific Antibody Status in Oral Fluids Modestly Reflects Serum Status in Human Immunodeficiency Virus-Positive Individuals. CVI
10: 431-438
[Abstract][Full Text]
Walker, F., Kermorgant, S., Darai, E., Madelenat, P., Cremieux, A. C., Henin, D., Lehy, T.
(2003). Hepatocyte Growth Factor and c-Met in Cervical Intraepithelial Neoplasia: Overexpression of Proteins Associated with Oncogenic Human Papillomavirus and Human Immunodeficiency Virus. Clin. Cancer Res.
9: 273-284
[Abstract][Full Text]
Eiben, G. L., Velders, M. P., Schreiber, H., Cassetti, M. C., Pullen, J. K., Smith, L. R., Kast, W. M.
(2002). Establishment of an HLA-A*0201 Human Papillomavirus Type 16 Tumor Model to Determine the Efficacy of Vaccination Strategies in HLA-A*0201 Transgenic Mice. Cancer Res.
62: 5792-5799
[Abstract][Full Text]
Kuntz, K. M., Goldie, S. J.
(2002). Assessing the Sensitivity of Decision-Analytic Results to Unobserved Markers of Risk: Defining the Effects of Heterogeneity Bias. Med Decis Making
22: 218-227
[Abstract]
Esiashvili, N., Landry, J., Matthews, R. H.
(2002). Carcinoma of the Anus: Strategies in Management. The Oncologist
7: 188-199
[Abstract][Full Text]
Goodman, A., Penson, R. T., Blatman, R., McIntyre, J., Gioiella, M. E., Chabner, B. A., Lynch, T. J. Jr.
(2002). A Staff Dialogue on a Socially Distanced Patient: Psychosocial Issues Faced by Patients, Their Families, and Caregivers. The Oncologist
7: 50-57
[Abstract][Full Text]
Kim, J. J., Wright, T. C., Goldie, S. J.
(2002). Cost-effectiveness of Alternative Triage Strategies for Atypical Squamous Cells of Undetermined Significance. JAMA
287: 2382-2390
[Abstract][Full Text]
Wright, T. C. Jr, Cox, J. T., Massad, L. S., Twiggs, L. B., Wilkinson, E. J., for the 2001 ASCCP-Sponsored Consensus Conference,
(2002). 2001 Consensus Guidelines for the Management of Women With Cervical Cytological Abnormalities. JAMA
287: 2120-2129
[Abstract][Full Text]
Clarke, B, Chetty, R
(2002). Postmodern cancer: the role of human immunodeficiency virus in uterine cervical cancer. Mol. Pathol.
55: 19-24
[Abstract][Full Text]
Mayaud, P., Gill, D. K, Weiss, H. A, Uledi, E., Kopwe, L., Todd, J., ka-Gina, G., Grosskurth, H., Hayes, R. J, Mabey, D. C., Lacey, C. J N
(2001). The interrelation of HIV, cervical human papillomavirus, and neoplasia among antenatal clinic attenders in Tanzania. Sex. Transm. Infect.
77: 248-254
[Abstract][Full Text]
Goldie, S. J., Kuhn, L., Denny, L., Pollack, A., Wright, T. C.
(2001). Policy Analysis of Cervical Cancer Screening Strategies in Low-Resource Settings: Clinical Benefits and Cost-effectiveness. JAMA
285: 3107-3115
[Abstract][Full Text]
Vecchione, A., Zanesi, N., Trombetta, G., French, D., Visca, P., Pisani, T., Botti, C., Vecchione, A., Croce, C. M., Mancini, R.
(2001). Cervical Dysplasia, Ploidy, and Human Papillomavirus Status Correlate with Loss of Fhit Expression. Clin. Cancer Res.
7: 1306-1312
[Abstract][Full Text]
Thomas, D. B., Ray, R. M., Kuypers, J., Kiviat, N., Koetsawang, A., Ashley, R. L., Qin, Q., Koetsawang, S.
(2001). Human Papillomaviruses and Cervical Cancer in Bangkok. III. The Role of Husbands and Commercial Sex Workers. Am J Epidemiol
153: 740-748
[Abstract][Full Text]
Hader, S. L., Smith, D. K., Moore, J. S., Holmberg, S. D.
(2001). HIV Infection in Women in the United States: Status at the Millennium. JAMA
285: 1186-1192
[Abstract][Full Text]
Scott, M., Nakagawa, M., Moscicki, A.-B.
(2001). Cell-Mediated Immune Response to Human Papillomavirus Infection. CVI
8: 209-220
[Full Text]
Liu, D.-W., Tsao, Y.-P., Hsieh, C.-H., Hsieh, J.-T., Kung, J. T., Chiang, C.-L., Huang, S.-J., Chen, S.-L.
(2000). Induction of CD8 T Cells by Vaccination with Recombinant Adenovirus Expressing Human Papillomavirus Type 16 E5 Gene Reduces Tumor Growth. J. Virol.
74: 9083-9089
[Abstract][Full Text]
Orjuela, M., Castaneda, V. P., Ridaura, C., Lecona, E., Leal, C., Abramson, D. H., Orlow, I., Gerald, W., Cordon-Cardo, C.
(2000). Presence of Human Papilloma Virus in Tumor Tissue from Children with Retinoblastoma: An Alternative Mechanism for Tumor Development. Clin. Cancer Res.
6: 4010-4016
[Abstract][Full Text]
Frisch, M., Biggar, R. J., Goedert, J. J.
(2000). Human Papillomavirus-Associated Cancers in Patients With Human Immunodeficiency Virus Infection and Acquired Immunodeficiency Syndrome. JNCI J Natl Cancer Inst
92: 1500-1510
[Abstract][Full Text]
Cubie, H A, Seagar, A L, Beattie, G J, Monaghan, S, Williams, A R W
(2000). A longitudinal study of HPV detection and cervical pathology in HIV infected women. Sex. Transm. Infect.
76: 257-261
[Abstract][Full Text]
Berkhout, R. J. M., Bouwes Bavinck, J. N., ter Schegget, J.
(2000). Persistence of Human Papillomavirus DNA in Benign and (Pre)malignant Skin Lesions from Renal Transplant Recipients. J. Clin. Microbiol.
38: 2087-2096
[Abstract][Full Text]
Kuhn, L., Denny, L., Pollack, A., Lorincz, A., Richart, R. M., Wright, T. C.
(2000). Human Papillomavirus DNA Testing for Cervical Cancer Screening in Low-Resource Settings. JNCI J Natl Cancer Inst
92: 818-825
[Abstract][Full Text]
Ryan, D. P., Compton, C. C., Mayer, R. J.
(2000). Carcinoma of the Anal Canal. NEJM
342: 792-800
[Full Text]
Petter, A., Heim, K., Guger, M., Ciresa-Kö nig, A., Christensen, N., Sarcletti, M., Wieland, U., Pfister, H., Zangerle, R., Höpfl, R.
(2000). Specific serum IgG, IgM and IgA antibodies to human papillomavirus types 6, 11, 16, 18 and 31 virus-like particles in human immunodeficiency virus-seropositive women. J. Gen. Virol.
81: 701-708
[Abstract][Full Text]
Ellerbrock, T. V., Chiasson, M. A., Bush, T. J., Sun, X.-W., Sawo, D., Brudney, K., Wright, T. C. Jr
(2000). Incidence of Cervical Squamous Intraepithelial Lesions in HIV-Infected Women. JAMA
283: 1031-1037
[Abstract][Full Text]
Moscicki, A.-B., Ellenberg, J. H., Vermund, S. H., Holland, C. A., Darragh, T., Crowley-Nowick, P. A., Levin, L., Wilson, C. M.
(2000). Prevalence of and Risks for Cervical Human Papillomavirus Infection and Squamous Intraepithelial Lesions in Adolescent Girls: Impact of Infection With Human Immunodeficiency Virus. Arch Pediatr Adolesc Med
154: 127-134
[Abstract][Full Text]
Burk, R. D.
(1999). Pernicious Papillomavirus Infection. NEJM
341: 1687-1688
[Full Text]
Dolei, A., Curreli, S., Marongiu, P., Pierangeli, A., Gomes, E., Bucci, M., Serra, C., Degener, A. M.
(1999). Human immunodeficiency virus infection in vitro activates naturally integrated human papillomavirus type 18 and induces synthesis of the L1 capsid protein. J. Gen. Virol.
80: 2937-2944
[Abstract][Full Text]
Savard, J., Miller, S. M., Mills, M., O'Leary, A., Harding, H., Douglas, S. D., Mangan, C. E., Belch, R., Winokur, A.
(1999). Association Between Subjective Sleep Quality and Depression on Immunocompetence in Low-Income Women at Risk for Cervical Cancer. Psychosom. Med.
61: 496-507
[Abstract][Full Text]
Critchlow, C. W., Kiviat, N. B.
(1999). Old and New Issues in Cervical Cancer Control. JNCI J Natl Cancer Inst
91: 200-201
[Full Text]
Palefsky, J. M., Minkoff, H., Kalish, L. A., Levine, A., Sacks, H. S., Garcia, P., Young, M., Melnick, S., Miotti, P., Burk, R.
(1999). Cervicovaginal Human Papillomavirus Infection in Human Immunodeficiency Virus-1 (HIV)-Positive and High-Risk HIV-Negative Women. JNCI J Natl Cancer Inst
91: 226-236
[Abstract][Full Text]
Goldie, S. J., Weinstein, M. C., Kuntz, K. M., Freedberg, K. A.
(1999). The Costs, Clinical Benefits, and Cost-Effectiveness of Screening for Cervical Cancer in HIV-Infected Women. ANN INTERN MED
130: 97-107
[Abstract][Full Text]
Mandelblatt, J. S., Kanetsky, P., Eggert, L., Gold, K.
(1999). Is HIV Infection a Cofactor for Cervical Squamous Cell Neoplasia?. Cancer Epidemiol. Biomarkers Prev.
8: 97-106
[Abstract][Full Text]
De Groot, A. S., Leibel, S. R., Zierler, S.
(1998). A Standard of HIV Care for Incarcerated Women: Northeastern United States' Experiences. J Correct Health Care
5: 139-177
[Abstract]
Fink, M. J., Goodman, A., Hight, E., Miller-Mack, E., De Groot, A.
(1998). Critical Prevention, Critical Care: Gynecological and Obstetrical Aspects of Comprehensive HIV Prevention and Treatment Among Incarcerated Women. J Correct Health Care
5: 201-223
[Abstract]
Lynch, H. T., Casey, M. J., Shaw, T. G., Lynch, J. F.
(1998). Hereditary Factors in Gynecologic Cancer. The Oncologist
3: 319-338
[Abstract][Full Text]
Vernon, S. D., Unger, E. R., Reeves, W. C., Frisch, M., Adami, H.-O., Melbye, M., Ellerbrock, T. V., Kuhn, L., Wright, T. C.
(1998). Human Papillomaviruses and Anogenital Cancer. NEJM
338: 921-922
[Full Text]
(1997). Human Papillomavirus in HIV-Infected Women. AIDS Clin Care
1997: 3-3
[Full Text]
(1997). Papillomavirus in HIV-Positive Women. JWatch Women's Health
1997: 2-2
[Full Text]
Shah, K. V.
(1997). Human Papillomaviruses and Anogenital Cancers. NEJM
337: 1386-1388
[Full Text]